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ACTAUNIVERSITATIS
UPSALIENSISUPPSALA
2017
Digital Comprehensive Summaries of Uppsala Dissertationsfrom the Faculty of Science and Technology 1506
Morphometric analysis ofCambrian fossils and itsevolutionary significance
ILLIAM JACKSON
ISSN 1651-6214ISBN 978-91-554-9894-8urn:nbn:se:uu:diva-319487
Dissertation presented at Uppsala University to be publicly examined in Norrlands 1 & 2,Villavägen 16, Uppsala, Friday, 2 June 2017 at 13:00 for the degree of Doctor of Philosophy.The examination will be conducted in English. Faculty examiner: Professor Nigel Hughes(University of California, Riverside).
AbstractJackson, I. 2017. Morphometric analysis of Cambrian fossils and its evolutionarysignificance. Digital Comprehensive Summaries of Uppsala Dissertations from theFaculty of Science and Technology 1506. 63 pp. Uppsala: Acta Universitatis Upsaliensis.ISBN 978-91-554-9894-8.
The Extended Evolutionary Synthesis (EES) is currently emerging as a theoretical alternativeto the Modern Synthesis (MS) in which to frame evolutionary observations and interpretations.These alternative frameworks differ fundamentally in their understanding of the relativeroles of the genotype, phenotype, development and environment in evolutionary processesand patterns. While the MS represents a gene-centred view of evolution, the EES insteademphasizes the interactions between organism, development and environment. This noveltheoretical framework has generated a number of evolutionary predictions that are mutuallyincompatible with the equivalent of the MS. While research and empirical testing has begun ona number of these in a neontological context, the field of palaeontology has yet to contributemeaningfully to this endeavour. One of the reasons for this is a lack of methodologicalapproaches capable of investigating relevant evolutionary patterns in the fossil record. In thisthesis morphometric methods capable of providing relevant data are developed and employedin the analysis of Cambrian fossils. Results of these analyses provide empirical support for theprocess of evolution through phenotypic plasticity and genetic assimilation hypothesized by theEES. Furthermore, theoretical revision to the species concept in a palaeontological context issuggested. Finally, predictions of the EES specific to the fossil record are made explicit andpromising directions of future research are outlined.
Keywords: Extended Evolutionary Synthesis, phenotypic plasticity, genetic assimilation,phenotypic accommodation, Agnostus pisiformis, Mackinnonia, elliptical fourier analysis,species concept
Illiam Jackson, Department of Earth Sciences, Palaeobiology, Villav. 16, Uppsala University,SE-75236 Uppsala, Sweden.
© Illiam Jackson 2017
ISSN 1651-6214ISBN 978-91-554-9894-8urn:nbn:se:uu:diva-319487 (http://urn.kb.se/resolve?urn=urn:nbn:se:uu:diva-319487)
For Steph
List of Papers
This thesis is based on the following papers, which are referred to in the text by their Roman numerals:
I Jackson, I. S. C. & Budd, G. E. (2017) Intraspecific morpholog-
ical variation of Agnostus pisiformis, a Cambrian Series 3 trilo-bite-like arthropod. Lethaia, published online 15 March 2017. doi:10.1111/let.12201
II Jackson, I. S. C. & Claybourn, T. M. (manuscript submitted to Palaeontology) Morphometric Analysis of the Early Cambrian mollusc Mackinnonia and the Incipient Species Concept.
III Jackson, I. S. C., Bohlin, M. S., Mann, R. P., Budd, G. E. (man-uscript submitted to Nature) Genetic assimilation in the fossil record: phenotypic plasticity and accommodation in Cambrian arthropods.
IV Jackson, I. S. C. & Budd, G. E. (manuscript) The Extended Evo-lutionary Synthesis in the fossil record.
Additionally, the following paper was prepared during the course of the PhD, but is not included in the thesis:
I Budd, G. E. & Jackson, I. S. C. (2016) Ecological innovations in the Cambrian and the origins of the crown group phyla. Philo-sophical Transactions of the Royal Society B 371, 20150287. doi:10.1098/rstb.2015.0287
Reprints were made with permission from the respective publishers.
Statement of authorship Paper I: I. J. collected the material and conducted the analyses, and interpreted the results and authored the paper with input from G. B. Paper II: I. J. analysed the material, and interpreted the results and co-authored the paper together with T. C. Paper III: I. J. collected material and conducted the morphometric analyses, and co-authored the bulk of the paper together with G. B. Paper IV: I. J. authored the paper with input from G. B.
Contents
Introduction ..................................................................................................... 9
Organismal variation is continuous .............................................................. 11 A brief history of classification ................................................................ 11 Phylogenetics ........................................................................................... 12 Morphometrics and stratophenetics .......................................................... 17 Morphometric methods ............................................................................ 22 Summary .................................................................................................. 23 Case study ................................................................................................ 23
The morphological variation of Mackinnonia .............................................. 24 Helcionelloida .......................................................................................... 24 Mackinnonia ............................................................................................. 24 Morphological variation and the incipient species concept ..................... 25
Natural selection acts on the phenotype ........................................................ 28 The level of selection ............................................................................... 28 The Extended Evolutionary Synthesis ..................................................... 29 Evolution through phenotypic plasticity and genetic assimilation ........... 31 Macroevolutionary patterns ...................................................................... 33 Quantum evolution ................................................................................... 35 Summary .................................................................................................. 39 Case study ................................................................................................ 40
The phenotypic plasticity of Agnostus pisiformis ......................................... 41 Agnostus pisiformis .................................................................................. 41 Intraspecific variation ............................................................................... 42 Patterns of phenotypic plasticity and genetic assimilation ....................... 43
Conclusion .................................................................................................... 47 Organismal variation is continuous .......................................................... 47 Natural selection acts on the phenotype ................................................... 47
Future directions ........................................................................................... 49 Morphometrics in the fossil record .......................................................... 49 Cambrian explosion .................................................................................. 49
Introduktion .............................................................................................. 51 Evolution genom fenotypisk plasticitet och genetisk assimilation ........... 52 Variation som ett kontinuerligt spektrum ................................................. 52 Morfologisk variation hos Mackinnonia .................................................. 53 Fenotypisk plasticitet och genetisk assimilation hos Agnostus pisiformis .................................................................................................. 53 Slutsatser och framtidsutsikter ................................................................. 54
Acknowledgements ....................................................................................... 55
References ..................................................................................................... 57
Svensk Sammanfattning ................................................................................ 51
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Introduction
Scientific research takes place within a theoretical framework, which can be defined as a set of implicit or explicit assumptions, conceptualizations and perspectives. This framework determines both the research questions that can be explored and the methods that can be developed. These are interdependent; novel perspectives permit the development of new methodologies and new methodologies make possible the investigation of novel research questions. It is essential, therefore, from time to time to critically review the framework in which a field of research is being conducted and to evaluate how this frame-work is affecting the scope and potential of the research within that field.
The Extended Evolutionary Synthesis (EES; Laland et al., 2015) is one such currently emerging reevaluation of a theoretical framework. Specifically it seeks to revise or extend the Modern Synthesis (MS) in evolutionary biol-ogy. Although this sounds dramatic, it is hardly the first time that such a revi-sion is called for, nor is it likely to be the last. In the midst of the debate on levels of selection during the late 20th century, Gould (1982) wrote that “cur-rent critics of Darwinism and the modern synthesis are proposing a good deal more than a comfortable extension of the theory, but much less than a revolu-tion”. Similarly, Laland et al. (2015) write that “the EES requires no ‘revolu-tion’” yet “nevertheless, our analysis suggests that the EES is more than simply an extension of ‘business as usual’ science: it requires conceptual change.” Now, like then, as Gould (1982) summarised: “the modern synthesis is incomplete, not incorrect.”
The conceptual change represented by the EES is chiefly a shift in focus from a gene-centered view of evolution to a more holistic understanding of the many complex relationships that exist between genotype, phenotype and environment, which together form the evolutionary processes and patterns that are studied in the fields of evolutionary biology. The work that I have con-ducted for this thesis is synergistic with this theoretical revision of the MS. I hope to show how new theoretical perspectives and conceptual frameworks can generate novel research by facilitating the investigation of previously un-available research questions.
This thesis is structured around two observations (or perhaps more fairly assertions) regarding evolution. They are both essentially Darwinian and un-controversial in principle, but I believe that they are currently incongruous with the theoretical framework of the MS. I hope to show that a return to a perspective incorporating their simple and empirical truths will contribute to the generation of informative research on current evolutionary topics.
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The first point regards the nature of organismal variation, which we ought to view as continuous and not discrete. I first establish how the history of clas-sification and evolutionary thought has introduced a deep-rooted bias to our conceptualization of variation that limits the research methods we can develop and consequently the research we can conduct. I then illustrate the utility of novel methodologies developed within a context that understands variation as continuous rather than discrete by providing an example of my work with the Early Cambrian mollusc Mackonnonia developing a novel framework with which to understand speciation processes (Paper II).
The second point regards the level at which natural selection operates, which we ought to view as the phenotype and not the genotype. I first discuss the contrasting perspectives of the EES and the MS in terms of levels of se-lection; relative roles of the genotype, phenotype and environment; and evo-lutionary significance of phenotypic plasticity and genetic assimilation. I ar-gue for the development of a theoretical framework that incorporates a more complex model of interaction between genotype and phenotype than that of the MS. I then exemplify the utility of such a framework by providing exam-ples of my work investigating subtle patterns of morphological variation, in-terpreted as signals of phenotypic plasticity and genetic assimilation, in Ag-nostus pisiformis, a Cambrian Series 3 trilobite-like arthropod, and its close relatives (Paper I & III).
I conclude by highlighting the manner in which the palaeontological meth-ods developed in my work and the conceptual perspectives discussed and ex-emplified throughout this thesis combine to provide great potential for novel research in the field of palaeobiology, provided theoretical frameworks such as the EES can formulate explicit testable predictions in the fossil record such as those presented in Paper IV.
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Organismal variation is continuous
A brief history of classification Our current synthetic understanding of evolution is summarised still in Dar-win’s “descent with modification” (Darwin, 1859); new organismal form evolves in evolutionary lineages as gradual variation on preceding form slowly generating phenotypic novelties. Why is it then that the prevailing con-ceptualization of the natural variation of animals and plants is into discrete units of species rather than portions of a continuous evolved and continuously evolving whole? The answer lies of course in the gaps of this spectrum of organismal variation. While evolution generates diversity, extinction creates disparity and it is these patterns of disparity that give structure to our under-standing of natural variation.
Figure 1. Bracketed tables. These hierarchical charts are read horizontally left to right and structure organismal variation in terms of perceived similarity. Left: Gessner’s (1555) classification of wading birds. Right: Wilkins’ (1668) classification of birds.
The identification and classification of nature’s varieties has always func-tioned thus; the disparity between organisms demarcate them from one an-other and provides the necessary atomisation of variation that is required to meaningfully compare and classify organisms. From Aristotle’s categories through the bracketed tables of the 16th and 17th century (Figure 1) to Lin-naeus’ binomial classification (1735), which still serves as an integral compo-nent of systematic analyses today, hierarchical structures of classification have revolved around the identification of features capable of differentiating groups of organisms. It was in this context that the organisms of the natural world were first categorised and organized according to their perceived degree of
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similarity in increasingly comprehensive works culminating in Linnaeus’ masterpiece Systema Naturae. Linnaeus’ standardized rank-based system of classification provided an ideal structure by which to categorise the morpho-logical variation observed in nature.
Figure 2. Evolutionary tress. Left: Lamarck’s (1815) understanding of animal evolu-tion organized into two “lineages”. Right: Darwin’s (1859) familiar illustration of evolution as a branching tree.
While early work classifying and grouping organisms according to their per-ceived morphological similarities occurred in a non-evolutionary context, once evolutionary theories such as those of Lamarck (1809) and Darwin (1859) were developed the relevance of such classification to the study of evo-lution was immediately apparent. It became clear that the patterns of similarity in the natural world that had been identified and mapped in fact held biologi-cally relevant information about the relatedness of organisms (Figure 2). Thus it was in this theoretical framework of conceptualizing organismal variation as discrete and of structuring evolutionary lineages along standardized ranks that the field of evolutionary biology was conceived. This is very significant because this framework continues to influence research carried out to this day.
Phylogenetics As understanding of evolutionary processes and patterns grew during the late 19th and early 20th century, the classification of organisms became the sci-ence of phylogenetics. However, incorporating evolution into a rank-based mode of classification that was originally created purely as a descriptive sys-tem has posed, and continues to pose, a number of challenges. For example, for a long time palaeontologists struggled with how to interpret fossils very
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dissimilar to extant fauna. The most famous example of this is in the interpre-tation of the Burgess Shale fauna. Gould’s (1989) understanding of the then bizarre-looking Burgess Shale fauna was undoubtedly structured in taxonomic terms when he interpreted it as representing the remnants of several high-level taxonomic groups that all had since gone extinct. This view mirrors the “phy-logenetic lawn” (Figure 3) of Whittington (1979) and suggests that the Cam-brian radiation of animals produced many more independent evolutionary lin-eages than previously imagined, most of which today are extinct. This natu-rally has enormous implications on our understanding of evolution’s most fun-damental aspects such as evolvability, constraints, developmental systems and the role of contingency (e.g. Gould, 1989; Conway Morris, 1998) and is dis-cussed in more detail further on in this thesis.
Figure 3. Conceptualization of morphologically strongly dissimilar organisms. Left: Whittington’s (1979) phylogenetic lawn; his illustration of arthropod diversity exhib-iting the shape of a grass lawn with many high-level taxa emerging in the early Pal-aeozoic only to die out relatively soon. This version redrawn in Briggs, 2015. Right: Budd & Jensen’s (2000) clarification of the stem and crown group concept providing a context in which seemingly morphologically bizarre fossils can be more construc-tively related to extant fauna.
It was not until Budd & Jensen’s (2000) revival of the stem- and crown group concept (Jefferies, 1979) that this fossil fauna assumed its correct position along the stem groups of extant phyla (Figure 3). This serves both as an ex-ample of the manner in which our conceptual framework structures our inter-pretation of observations as well as an example of how the history of the meth-odologies and nomenclature that we adopt sometimes render them counter-productive. In this instance the purely descriptive function of the rank-based classification system interfered with its evolutionary function. In other words, strongly dissimilar morphologies are best expressed through differences at higher taxonomic levels, yet this has evolutionary implications when such ranks are imbued with phylogenetic meaning. While the stem- and crown group concept resolved this particular problematic artefact of our system of
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classification, this incongruence between the dual functionality of taxonomic ranks in an evolutionary context was neither the first nor the last conceptual issue encountered during the development of modern systematics.
Earlier, during the beginning of the 20th century, the nascent field of evo-lutionary biology grappled with the existential issue of how our classification of organismal variation related to the empirical world; was our conceptualiza-tion of taxa merely a human construct or did it reflect something that existed physically in reality, and if so what was that thing? This problem became known as the “species problem” (Wilkins, 2004) and still represents a philo-sophical challenge to evolutionary biologists (Pigliucci, 2003; de Queiroz, 2005; Hey, 2006; de Queiroz, 2007); are species, and indeed taxa, purely de-scriptive and hence subjective or can they be objectively delimited?
During the formation of the Modern Synthesis (Huxley, 1942), Dobzhan-sky (1935; 1937) and Mayr (1942) together formalized what is today known as the biological species concept (Coyne, 1994) in an attempt to resolve this issue. However, this resolution was framed in a neontological context and has since caused enduring theoretical difficulties for palaeontologists (Allmon, 2016; Miller, 2016). Mayr (1942), for instance, defines species as “groups of actually or potentially interbreeding natural populations, which are reproduc-tively isolated from other such groups”. While the relevance of such a defini-tion to a population geneticist or ecologist is immediately apparent, it is cer-tainly less useful to a palaeontologist, whose objects of study provide little to no information on interbreeding or the potential thereof. Mayr (1942) noted this problem and concludes that “the ‘species’ of the paleontologist is not nec-essarily always the same as the ‘species’ of the student of living faunae”. It was in this context focused chiefly on microevolutionary processes that Simp-son (1944) brought palaeontology into the Modern Synthesis.
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Figure 4. Simpson’s (1944) illustration of palaeontological populations evolving through time. Each curve represents a successive population and the dashed lines il-lustrate phylogeny.
Simpson illustrated clearly the relationship between the microevolutionary processes summarised in the Modern Synthesis and the macroevolutionary patterns that follow in the fossil record. His remarkable synthesis of these con-texts is notable also for the manner in which he discretizes the process of evo-lution (Figure 4). Rather than illustrating evolution as a fluid transition along a spectrum of variation, it is illustrated as a sequence of increasingly dissimilar populations. Owing perhaps to the incompleteness of the fossil record as well as the theoretical context of the time, this representation of evolution can nev-ertheless be seen as a continuation of the tradition of understanding variation in discrete terms. Indeed Mayr (1942) rejects the notion of systematic units such as species as abstractions stating explicitly that “such a unit is objective, or real, if it is delimited against other units by fixed borders, by definite gaps.”
The imperfection of the geological record seen already by Darwin (1859) as “perhaps [...] the most obvious and serious objection which can be urged against the theory [of evolution]” is contrasted by Mayr (1942) who describes it as “convenient gaps between the ‘species’”. He writes: “In the few cases, in which an almost complete record of a continuous [evolutionary] line is already available, the paleontologist follows the reasoning of the taxonomist who is confronted with an unbroken intergrading series of geographic populations. [They] [break] them up for convenience.” (Mayr, 1942). This exemplifies ex-plicitly the manner in which organismal variation is understood in discrete terms; those rare cases where we in fact possess a continuous record of evolu-tion are discretized in any case!
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This understanding of variation as discrete was foundational for the later development of cladistics as the primary mode of phylogenetic analysis during the second half of the 20th century (e.g. Hennig, 1966; Farris, 1970; Farris et al., 1970). The idea of transforming phylogenetic analysis into an essentially mathematical operation was revolutionary and epitomized by the notion of developing a system of analysis that an “intelligent ignoramus” could operate (Sokal & Sneath, 1966; Sokal & Rohlf, 1970). This translation of the mode of species and taxa delimitation necessitated the development of a specifically phylogenetic species concept as an alternative to that of Mayr and Dobzhan-sky mentioned above (Cracraft, 1983).
The phylogenetic species concept defines a species as “an irreducible (ba-sal) cluster of organisms that is diagnosably distinct from other such clusters, and within which there is a parental pattern of ancestry and descent” (Cracraft, 1989). The feature that differentiates species or clusters in this sense is “a unique combination of character states in comparable individuals.“ (Nixon & Wheeler, 1990). In other words, cladistic analysis relies on the identification of characters and character states, which are used to construct evolutionary trees according to various criteria. While the identification of characters for use in such analyses initially occurred on an ad-hoc basis (Fristrup, 2001), the concept of the character has seen recent theoretical exploration (Wagner, 2000; McShea & Venit 2001). However, character state identification contin-ues to prove challenging chiefly because of the inherent difficulty of translat-ing continuous variation of characters into discrete states (Stevens, 1991; Gift & Stevens, 1997).
One of the more problematic aspects of this mode of phylogenetic analysis is the inherent loss of data. The translation of continuous organismal variation into first a set of discrete characters and then a set of discrete states within those characters represents a strong reduction in resolution of data available for analysis. In particular, this poses a challenge to the field of palaeontology where morphological variation is essentially the only source of evolutionary information. Strongly reducing the resolution of the morphological variation in the fossil record restricts the investigations that can be conducted and hence the research questions that can be answered. For example, comparative anal-yses of organisms that exhibit few or no qualitatively different characters can-not be satisfactorily conducted in a cladistic context presenting a serious dif-ficulty to the study of intraspecific variation and related research questions. So while cladistics as a phylogenetic method has contributed greatly to the clarification of the relationship between broader groups of organisms and their evolutionary patterns, it struggles to examine evolutionary patterns at a closer level.
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Morphometrics and stratophenetics If the understanding of morphological variation as discrete is a natural result of the historical context of evolutionary biology, as I hope I have shown, then morphometrics, the quantitative study of morphological variation, represents a revolutionary conceptualization of variation. In particular morphometrics offers great potential to the field of palaeontology where, as mentioned above, morphology is essentially the only source of information. Viewing morpho-logical variation in terms of continuous spectra rather than discrete categories or characters permits both the development of novel methodologies as well as the investigation of novel hypotheses. Before discussing such morphometric methodologies, I first outline the development of this conceptualization of evolution.
Figure 5. Matthew’s (1930) phylogenetic tree of dogs illustrating their relationships with bears and raccoons.
The notion of depicting variation along spectra of variation occurs intermit-tently throughout the history of evolutionary biology but has not yet been fully developed as a phylogenetic method. Early illustrations of evolutionary rela-tionships such as that of Matthew (1930) are just that; illustrations (Figure 5). Matthew’s (1930) depiction of the evolutionary history of the canids expresses morphological variation along its x-axis although this is not to any scale or unit. Milne & Milne’s (1939) beautiful illustration of the phylogeny of cad-disflies (remarkable also for its three-dimensional approach presenting both ecological and morphological information against time) explicitly states that
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the x-axis represents morphological similarity, although also does not provide any scale or unit (Figure 6).
Figure 6. Milne & Milne’s (1939) evolutionary tree of caddisflies depicting morpho-logical variation through time. Ahead of its time, this tree also depicts degree of eco-logical differentiation along the y axis.
Further development of this idea is exemplified by Sokal and Sneath (1965), who illustrated evolution three-dimensionally using both x and y axes as measures of morphological similarity (Figure 7). While still theoretical in na-ture, this work helped develop the concept of a morphospace; a spectrum of the morphological variation of organisms or their features. While Matthew’s illustration of evolution depicted patterns between discrete groups (Figure 5),
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those of Milne & Milne (Figure 6) and Sokal & Sneath (Figure 7) describe morphological variation and, chiefly, morphological evolution in continuous terms. This is very significant because it highlights the incongruence between the prevalent understanding of species as discrete units and the nature of evo-lution as a continuous process.
Figure 7. Sokal & Sneath (1965) used this diagram to illustrate how a purely phenetic approach to mapping evolution could mistakenly identify convergent evolution in X as a phylogenetic signal for its affinity to B rather than its true affinity to A. This was in reference to the debate between pheneticists and cladists (see Weygoldt, 1979 for a summary).
Indeed, one of the reasons that the study of evolution in this theoretical frame-work was never popularized is due to the lack of methodologies developed from this perspective. The most notable attempt at developing a methodology for studying evolution in these terms is Gingerich’s stratophenetic approach (1979). He described this approach as “[combining] stratigraphic evidence of
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relative temporal position with phenetic clustering and linking to yield an es-sentially empirical reading of phylogeny.” His illustration of this conceptual-ization of evolution contains evolutionary patterns labeled as lineages (Figure 8) rather than species or taxa names.
Figure 8. Gingerich’s (1979) stratophenetic approach to mapping morphological var-iation through time. Successive assemblages of separate lineages are identified as sep-arate entities when a nonarbitrary morphological discontinuity forms between them such as between A and B. The boundary highlighted between B and C is arbitrary as it does not definitively separate the two assemblages.
Understanding that patterns of change through time occur along lineages ra-ther than via a set of discrete taxa is fundamental to the understanding and analysis of evolution in continuous terms. As an attempt to solve the species problem and synthesize the many disparate concepts of species, including the two outlined above, de Queiroz (2005) discusses and presents the metapopu-lation lineage concept. This explicit conceptualization of evolution as organ-ismal variation along a lineage echoes Gingerich’s stratophenetics (Figure 9).
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Figure 9. de Queiroz’ (2005) illustration of evolution of successive populations through time along an evolutionary lineage. While the illustration can be viewed two-dimensionally, representing three successive cross-sections of this lineage, it can also be viewed three-dimensionally, thus conceptualizing and emphasizing the continuous nature of morphological variation, cf. Figure 4.
Fossil assemblages thus represent cross-sections of such lineages. When as-semblages are analysed using morphometric methods, their variation is ex-pressed quantitatively along continuous spectra and thus stratophenetic pat-terns such as those imagined by Gingerich (Figure 8) can be meaningfully compared and phylogenetic patterns can be mapped. It is necessary to note at this point that while the assemblages of the fossil record are analogous to the populations of neontological studies there is a degree of time-averaging in fossil assemblages. This means that while populations are composed of con-temporaneous individuals sharing a geographic range, assemblages are com-posed of a succession of such populations. Thus, this time-averaging “prevents the detection of short-term (seasons, years) variability but provides an excel-lent record of the natural range of community composition and structure over longer periods.” (Kidwell & Flessa, 1995). For this reason assemblage, not population, is the correct term when discussing successive cross-sections of a lineage in the fossil record.
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Morphometric methods One of the limits to the stratophenetic approach at the time of its inception was the methods available for quantifying morphology. Early work by Gingerich and others mapped single metrics of successive assemblages through time (Figure 10). Modern morphometric methods, however, afford researchers far greater capabilities of reducing complex variation in shape and form to nu-merical values and thus axes of continuous variation mapped through time can contain more information than e.g. size or length.
Figure 10. Gingerich & Simons’ (1977) stratophenetic description of the evolution of Adapidae, a family of early primates. The x axis is a measurement of tooth size, used to infer relative body size. The variation of tooth size per assemblage is given as the black lines and the numbers next to each assemblage give the sample size.
Modern methods include landmark analyses (Bookstein, 1997) eigenshape analysis (MacLeod, 2002) and elliptical Fourier analysis (EFA; Kuhl & Giardina, 1982). Each of these provide the capacity, in particular when used in combination with multivariate analyses such as principal component anal-ysis (PCA), to condense morphological variation into few numerical values providing the real possibility of constructing Gingerich’s three-dimensional stratophenetic evolutionary tree (Figure 8) using empirical data.
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Summary I hope that I have shown that the understanding of organismal variation as continuous and not discrete is more than simply a semantic point; our concep-tualization of evolution and morphological variation provides structure to our theoretical framework, which defines the methods that we can develop and consequently the research questions that we can investigate. For this reason, the development of stratophenetic and morphometric methodologies will be useful for expanding our understanding of evolution.
Constructing evolutionary lineages based on perceived patterns in the fossil record is of course problematic. Gee (1998) writes that: “to take a line of fos-sils and claim that they represent a lineage is not a scientific hypothesis that can be tested, but an assertion that carries the same validity as a bedtime story—amusing, perhaps even instructive, but not scientific.” However, the development of a mode of phylogenetic analysis that studies patterns of con-tinuous morphological variation in fact represents the potential to test pre-cisely such assertions quantitatively.
Such an analysis will provide answers on how likely are our inferences of evolutionary relationships. The incompleteness of the fossil record will natu-rally continue to act as a limitation: “where the fossil record is dense and con-tinuous, a relatively clear pattern of genealogy emerges, but where there are large gaps in the record, the pattern is often ambiguous, a warning against any strong statement of relationships in such a case.” (Gingerich, 1979). Yet this is true for all phylogenetic methods of analysis and a stratophenetic approach is in fact likely to make explicit such limitations when present.
Case study In the next section I discuss Paper II in relation to the above and discuss how the patterns of morphological variation in Mackinnonia can help develop the theoretical framework of viewing organismal variation as continuous rather than discrete. Specifically, I discuss how novel morphometric methods help identify patterns of speciation in the fossil record and structure such patterns theoretically. Also I discuss the incipient species concept.
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The morphological variation of Mackinnonia
Helcionelloida Helcionelloids are univalved molluscs with a geological record spanning pre-trilobitic Cambrian Series 2 rocks (Kouchinsky et al. 2012, Matthews & Mis-sarzhevsy 1975) to the Early Ordovician (Gubanov & Peel 2001, Peel & Horný 2004). Their exact phylogenetic position is unclear. They have been placed variably in the gastropods (Parkhaev 2002), as a sister group to them (Lindsey & Kier 1984) or in a separate taxon with affinities to the mono-placophorans (Peel 1991). One of the reasons for this difficulty in determining their phylogeny is their preservation. Typically only internal moulds are found (Creveling et al 2014), which preserve as imprints of the microstructure of the internal shell, with many aragonitic crystal morphs (Kouchinsky 2000, Ven-drasco et al 2010, Vendrasco & Checa 2015). Whether or not the moulds re-covered truly represent the original organism is also unclear; it has been sug-gested that the moulds in fact represent juvenile forms of a much larger adult organism (Mart-Mus et al 2008, Jacquet & Brock 2016).
Mackinnonia Mackinnonia Runnegar in Bengtson 1990 is a morphologically variable (Parkhaev in Gravestock 2001) helcionelloid, known globally from the late Terreneuvian to Cambrian Series 2. In Paper II, specimens from three assem-blages of Mackinnonia are studied from Cambrian Series 2 Stages 3 and 4 rocks (Figure 11). Two of these are assemblages of Mackinnonia rostrata, from the Ajax Limestone in the Mount Scott Range, South Australia, and the Shackleton Limestone of East Antarctica. The third assemblage is of Mackin-nona taconica of the upper Bastion Formation of north-east Greenland.
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Figure 11. Mackinnonia from Paper II (A-C) Mackinnonia rostrata Zhou et Xiao 1984 from the Shackleton Limestone, East Antarctica (D-F) M. rostrata from the Ajax Formation, South Australia (H-I) Mackinnonia taconica Landing et Bartowski 1996 from the Bastion Formation, north-east Greenland. All scale bars are 200 µm.
Morphological variation and the incipient species concept Because the three assemblages of Mackinnonia exhibit a strongly similar mor-phology, a quantitative understanding of their morphological variation pro-vides the opportunity to detect what differences may exist between them. Pa-per II employs morphometric methods of analysing these assemblages in two ways, both using an approach involving EFA and PCA.
Firstly, the protoconchs, the parts of the moulds representing the larval stage of their development, are delimited and measured, and then compared across assemblages in a common morphospace. Secondly, each specimen is mapped ontogenetically using a novel approach that identifies successive
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growth stages and plots the specimens’ trajectories through these in a common morphospace. Using not only shape variation alone but also variation in shape change across ontogenetic trajectories is a very promising method showcased in this paper and is likely to be also useful for providing delimitation of spec-imens of other morphologically similar species and assemblages.
However, in this instance it is established that the shape of the protoconch alone is sufficient to not only distinguish between specimens of M. taconica and M. rostrata, but also to distinguish between the two assemblages of M. rostrata. The fact that these methods can identify significant morphological variation between specimens that have previously been described as the same species provides support for the notion that an understanding of organismal variation as continuous and not discrete provides the opportunity to explore new research questions. In this instance, it allows for the identification of sig-nificant intraspecific variation of M. rostrata and provides the potential for further exploration of these patterns and their causes.
Figure 12. Incipient species concept from Paper II. Incipient species are quantita-tively significantly different from one another but lack distinguishing qualitative fea-tures.
Paper II also interprets these findings in a theoretical context by exploring the relevance of this intraspecific variation to the species concept in palaeon-tology. The two assemblages of M. rostrata are identified as representing two groups of organisms in the early stages of speciating. Their qualitatively sim-ilar yet quantitatively significantly different morphology is used to define the incipient species concept (Figure 12); “incipient species are populations (or assemblages) of a species that exhibit minor or no morphological differences in terms of characters but significantly different morphology in quantitative
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terms.” (Paper II). This distinction, and consequently any research questions that derive from it, is a further example of the novel areas of research that present themselves to a perspective of organismal variation as continuous and not discrete.
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Natural selection acts on the phenotype
The level of selection Our understanding of natural selection is fundamentally unchanged since Dar-win (1859) wrote that it is “daily and hourly scrutinising [...]; silently and in-sensibly working [...] at the improvement of each organic being in relation to its organic and inorganic conditions of life.” The selective pressure of natural selection is the driving force behind evolution; organisms well-adapted to their environment survive to pass on their genes while others do not. Yet what it is precisely that nature is selecting has remained a controversial point in evolu-tionary biology. The debate on this matter has its roots in the generality of the “logical skeleton” of Darwin’s theory of evolution:
“1) Different individuals in a population have different morphologies, physi-ologies, and behaviors (phenotypic variation). 2) Different phenotypes have different rates of survival and reproduction in different environments (differential fitness). 3) There is a correlation between parents and offspring in the contribution of each to future generations (fitness is heritable).” (Lewontin, 1968)
Lewontin (1970) explains that:
“No particular mechanism of inheritance is specified, but only a corre-lation in fitness between parent and offspring. [...] Nor does Principle 2 specify the reason for the differential rate of contribution to future gen-erations of the different phenotypes. [...] This axiomatization makes clear that the principles can be applied equally to genes, organisms, populations, species, and at opposite ends of the scale, prebiotic mole-cules and ecosystems.”
This generality of the mode of transition of phenotypic variation provides the context for the concept of group selection (Vrba, 1984; Lloyd & Gould, 1993; Lieberman, 1995; Rabosky & McCune, 2010; Chevin, 2016). However, whether or not selection at higher levels, i.e. selection on groups contra indi-viduals, truly occurs and hence is a meaningful field of study is still an unre-solved issue (Hull, 1980; Sober & Lewontin, 1982; Vrba & Gould, 1986; Brandon, 1999; Reeve & Keller 1999; Clarke, 2010).
Connected to the debate on the concept of group selection is the notion of the “selfish gene” (Dawkins, 1976) and the idea that the process of evolution
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is instead ultimately reducible to a genetic level. Dawkins (1976) likens genes to “gigantic lumbering robots, sealed off from the outside world, communi-cating with it by tortuous indirect routes, manipulating it by remote control.” However, this view of the genotype as a “black box”; a simple generator of phenotypes, is increasingly being challenged by our growing understanding of the complex relationship between the genotype and phenotype (Noble, 2008; Pigliucci, 2010; Noble, 2015a; Laland et al., 2015). Noble argues that Dawkins' suggestion that “an organism is a tool of DNA rather than the other way round” (1982) is a polemic and not a scientific point by exemplifying the manner in which the opposite position produces a contradiction that is exper-imentally unresolvable: “an organism is the only tool by which DNA can ex-press functionality” (Noble, 2006).
West-Eberhard (2003) argues that it is absurd to argue that the genotype, rather than phenotype, is the object of selection:
“The misleading belief that the genotype is the focus of selection invites the idea that an individual genotype has a measurable fitness that is somehow intrinsic to itself (the naked genes) rather than being entirely a secondary consequence of the fitness or of reproductive success of the collective phenotypes it produces across life stages and in different en-vironments.”
This notion highlights the evolutionary significance of the emergent properties of the phenotype in its various contexts and reveals the fundamental philo-sophical difference between the reductionist gene-centered and the holistic phenotype-centered views of evolution. This debate on the conceptualization of natural selection and its operation is much more than a philosophical or semantic one; it is completely central to our understanding of evolution. At the heart of the issue are the perceived roles of, and relationships between, the genotype, phenotype and environment; a central theme of the Extended Evo-lutionary Synthesis (EES).
The Extended Evolutionary Synthesis The EES is a currently developing extension of the Modern Synthesis (MS), our current understanding of evolution (Laland et al., 2015). This theoretical extension is multifaceted but can be summarised by its focus on the themes of constructive development (Figure 13) and reciprocal causation and their im-plications for development and consequently for evolution. The necessity of such a theoretical extension is a currently highly contentious topic (Laland et al., 2014; Noble 2015a; Welch 2017).
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Figure 13. Contrasting views of development from Laland et al. (2015) (a) A unidi-rectional relationship between genotype and development in which the genotype of an organism is conceptualized as a blueprint for the generation of a given phenotype (b) A more inclusive understanding of development in the theoretical framework of the EES in which the genotype serves as a component of a developmental system taking cues from the environment and exhibiting more complex patterns of feedback.
A major difference between the frameworks of the MS and the EES is the level of perceived independence of the genotype. The MS considers the gen-otype as a “blueprint” for a phenotype and hence the relationship between genotype and phenotype is unidirectional. Evolutionary novelty is generated through the gradual accumulation of random mutations to the genotype and the environment’s function is to exert selective pressure on the resulting phe-notypic variation (Figure 13a). However, the EES assigns a far greater degree of complexity to organismal development (Figure 13b). In this view organis-mal development is not an independent process, isolated from external factors, but rather takes cues also from environmental factors (Keller, 2014). This pre-sents a wide range of potential sources of phenotypic novelty and variation because patterns of development become part of a biological system rich in feedback. For example, niche construction becomes more than the end product of genetic expression, but is also considered a process by which the environ-ment and hence the development of other organisms is altered (Odling-Smee et al., 2003). Including niche construction in the definition of an organism’s phenotype is analogous to Dawkins’ “extended phenotype” concept (1982). However, while Dawkins conceptualizes natural selection as merely selecting
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for those extended phenotypes that are best adapted for their environment, the EES assigns an agency of those extended phenotypes in structuring and di-recting natural selection itself.
Furthermore, progress in the field of evolutionary development (evo-devo) has revealed that gene regulatory networks (GRNs) provide an underlying ar-chitecture and modularity to organismal development (Davidson & Erwin, 2006; Müller, 2007; Brakefield, 2011). This has very significant implications in terms of the evolvability of organisms, the origin of phenotypic novelty and the patterns of evolution in general (Budd, 2006; Wagner & Zhang, 2011). Not least because such GRNs may be sensitive to environmental cues (Schnei-der & Meyer, 2017). Such cues facilitate the expression of phenotypic plas-ticity; the capacity of the same genome to generate varying phenotypes de-pending on environmental conditions. This interaction in effect offers the po-tential to “decouple” the genome from the phenotype essentially shielding the genome from selection; because the survival of an organism and consequently its genome depends on how well-adapted it is to its environment, the ability of the same genotype to generate a variety of phenotypes effectively shields the genotype from the selective pressures it would otherwise endure would it not have had such a capacity (Schlichting & Smith, 2002). This interaction reveals the importance of recognizing that selection occurs at the level of the phenotype, and not the genotype; selection is not for any one specific genotype but for that or those genotypes that can generate a phenotype well-adapted to its environment. This distinction is central for the following discussion on phenotypic plasticity and genetic assimilation.
Evolution through phenotypic plasticity and genetic assimilation The mechanism by which phenotypic plasticity operates has been explored theoretically (e.g. West-Eberhard, 2003; Crispo, 2007; Lande, 2009) but has proven difficult to establish empirically (McGuigan & Sgrò, 2009). As men-tioned above, our current understanding is that environmental triggers induce responses in GRNs thus altering organismal development (Gibson & Dworkin, 2004; Badyaev, 2005; Pigliucci et al. 2006; Schlichting 2008; Schneider & Meyer 2017). This provides the potential for environmental con-ditions or stresses to uncover previously unexpressed variation, also known as cryptic genetic variation (CGV; Gibson & Dworkin, 2004).
The role of CGV in evolution is a central topic of ongoing research in the EES framework (Laland et al., 2015). Mechanisms that lead to its accumula-tion and release are currently being explored (Schlichting 2008; Lande, 2009; Iwasaki et al., 2013; Schneider & Meyer 2017). Examples of patterns hypoth-
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esized to bring about such accumulation include stabilizing selection (Schmal-hausen, 1949) and genetic canalization (Waddington, 1942). Both of these concepts describe a pattern of organisms well-suited to their environment ex-hibiting a reduction of phenotypic variation. This reduction can be seen as adaptive; organisms that are well-suited to their environment are benefited by reliably reproducing the same phenotype despite perturbations to development or the environment. At a process level this is achieved through the buffering of development against the environmental cues discussed above (Schlichting & Smith, 2002); when development becomes more fixed in this manner it is considered genetically canalized (Figure 14).
Figure 14. The epigenetic landscape from Waddington, 1957. Development is imag-ined as a ball rolling down a landscape formed of channels and ridges (developmental pathways) until it reaches a stable point (resulting phenotype). When these channels deepen and ridges rise, development is said to become more canalized and will more reliably generate the same phenotype despite fluctuations to minor features of the landscape. When organisms are well-adapted to their environment, selection is for greater canalization. Environmentally induced changes to GRNs potentially radically alter the epigenetic landscape.
An effect of this buffering is that the same phenotype is produced despite fluc-tuations to the genotype, thus shielding a greater portion of the genome from selection facilitating the generation of CGV (Waddington, 1961; Rutherford, 2000; Badyaev, 2005; Schlichting, 2008; Schneider & Meyer 2017). The CGV that accumulates in organisms during such periods can later be released in response to strong environmental triggers that induce a response in GRNs as discussed above. Thus CGV can be understood as an evolutionary capacitor
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(Rutherford, 2000) and is hypothesized to play a central role in adaptive radi-ations (Schlichting 2008; Schneider & Meyer 2017) and in the generation of phenotypic novelty (West-Eberhard, 2003; Iwasaki et al., 2013).
One of the ways in which this can occur is through genetic assimilation, or phenotypic accommodation (Badyaev, 2009); ”a process by which characters which were originally ‘acquired characters’ may become converted, by a pro-cess of selection acting for several or many generations on the population con-cerned, into ‘inherited characters’.” (Waddington, 1961). This process has re-mained controversial ever since Waddington’s (1942) original experiments in which environmentally induced phenotypic variation became fixed as herita-ble traits in Drosophila (Pigliucci, 2007). However, in light of new theoretical approaches, empirical data is beginning to emerge supporting this process (Wund et al., 2008; Badyaev, 2009). In brief, environmental stresses are im-agined to induce changes to organisms’ epigenetic landscape thus expressing novel developmental pathways (Waddington, 1957; Figure 14). If such novel pathways and their consequential phenotypes are adaptive then natural selec-tion can select for their permanence (Noble, 2015b). These phenotypes are then genetically accommodated in the organism and their underlying genetic variation assimilated (West-Eberhard, 2005). The environment is thus respon-sible for the “simultaneous induction and selection of functional variants.” (Laland et al., 2015).
This is a theoretically challenging mode of evolution that critically neces-sitates the comprehension of the complex relationship between genotype, phe-notype and environment. Primarily it reminds us that natural selection acts on the phenotype of an organism and not the genotype. This distinction provides the necessary perspective to fully appreciate the prediction of the EES that “phenotypic accommodation can precede, rather than follow, genetic change, in adaptive evolution” (Laland et al., 2015).
Macroevolutionary patterns If the process of evolution through phenotypic plasticity and genetic assimila-tion as outlined above does indeed occur then a number of predictions of the resulting macroevolutionary patterns in the fossil record can be made. This is the specific topic explored in detail in Paper IV and so is discussed here in a more historical context.
The evolutionary process described above predicts, in short, two major pat-terns of evolution:
1. Stabilizing selection during periods of environmental stability leading to
decreasing phenotypic variation and genetic expression but the accumula-tion of CGV.
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2. Episodes of phenotypic plasticity induced by environmental stress facili-tating accelerated adaptive shifts and the generation of phenotypic novelty via the release of CGV.
With our contemporary understanding of developmental systems and the po-tential role of CGV discussed above, patterns of evolution in the fossil record previously difficult to explain can be interpreted in a new light. For example, the concept of punctuated equilibria (Eldredge & Gould, 1972; Gould & El-dredge, 1977) is easily related to the process described above. Radiative bursts of evolution exhibited during the punctuated equilibria can be understood as the episodic accelerated adaptive shifts facilitated by the environmentally in-duced release of CGV and consequent phenotypic variation (2), and intermit-tent stases of evolution as the periods of stabilizing selection during which development is canalized and CGV is regenerated (1). The process of evolu-tion through phenotypic plasticity followed by genetic assimilation of result-ing variation is thus in fact coherent with observed patterns of phenotypic evo-lution in the fossil record; natural selection operating on pulses of phenotypic variation resulting from the release of CGV would result in precisely the oc-currences of punctuated equilibria as described by Eldredge & Gould (1972).
However, genetic assimilation, i.e., the integration of environmentally in-duced phenotypes into the genome, has an almost century-old history of being categorically dismissed. Dawkins (2004) states unequivocally that “experi-mentally induced changes in bodies are never correlated with changes in genes, but changes in genes (mutations) are sometimes correlated with changes in bodies (and all evolution is the consequence).” His view that evo-lution occurs only through genetic mutations echoes the position of Mayr (1963): “all evolution is due to the accumulation of small genetic changes, guided by natural selection”. Why precisely genetic assimilation has remained so controversial ever since the formation of the Modern Synthesis is unclear, although Pigliucci et al. (2006) offer some potential explanation:
“We suggest that much of the controversy hinges on several misunder-standings, including unwarranted fears of a general attempt at over-throwing the Modern Synthesis paradigm, and some fundamental con-ceptual confusion about the proper roles of phenotypic plasticity and natural selection within evolutionary theory.”
Added to this list ought to be also the spectre of “Lamarckism”, falsely seen as embarrassing, looming still over evolutionary biology. In any case Simpson (1965) was correct in writing that “the inheritance of acquired characters [...] has been almost universally discarded by biologists.” and despite recent ad-vances this remains the case to a large extent today. However, it is ironic that Simpson notes on the issue because, as I hope to show below, his observations of what he termed “quantum evolution” (1944) provide some of the earliest
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interpretations of evolution through phenotypic plasticity and genetic assimi-lation!
Quantum evolution Gould (1986) highlights the manner in which Simpson’s writings on quantum evolution gradually disappear from his work during what he terms the “hard-ening of the Modern Synthesis”. In Tempo and Mode in Evolution (1944) Simpson defines quantum evolution, one of the three modes of evolution out-lined in the final chapter, as:
“The relatively rapid shift of a biotic population in disequilibrium to an equilibrium distinctly unlike an ancestral condition. Such a sequence can occur on a relatively small scale in any sort of population and in any part of the complex evolutionary process. It may be involved in either speciation or phyletic evolution, and it has been mentioned that certain patterns within those modes intergrade with quantum evolu-tion.”
Although he characterizes this mode of evolution as occurring typically at a “high taxonomic level”, he also stresses that “it can give rise to taxonomic groups of any size and the sequences involved can be (subjectively) divided into morphological units of any desired scope, from subspecies up.” (1944). Quantum evolution in his understanding occurred in three phases:
“1) An inadaptive phase, in which the group in question loses the equi-librium of its ancestors or collaterals. 2) A preadaptive phase, in which there is great selection pressure and the group moves toward a new equilibrium. 3) An adaptive phase, in which the new equilibrium is reached.” (Simp-son, 1944)
Simpson saw quantum evolution as not merely representing a faster version of phyletic evolution but an essentially different form of evolution. This is clear from the comparison he draws up of the characteristics of his modes of evolution (Simpson 1944), key features of which are reproduced here (Tables 1 & 2).
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Table 1. Simpson’s quantum evolution contrasted with “regular” phyletic evolution.
Mode Adaptive Type Direction Typical Patterns Stability
Phyletic evolution
Postadaptation and secular adaptation ; (little inadaptive or random change)
Commonly linear as a broad aver-age, or fol-
lowing a long shifting path
Trend with long-range modal shifts among bundles of multiple isolated
strands, often forked
Whole system shifting in es-sentially con-tinuous equi-
librium
Quantum evolution
Preadaptation (often preceded by in-
adaptive change)
More rigidly linear, but relatively
short in time
Sudden sharp shift from one position to
another
Radical or rel-ative instability with the sys-
tem shifting to-ward an equi-librium not yet
reached
Table 2. Simpson’s quantum evolution contrasted with “regular” phyletic evolution.
Mode Variability Typical Morpho-logical Changes
Typical Popula-tion Involved
Usual Rate Distribution
Phyletic evolution
Nearly con-stant in level;
most new vari-ants elimi-
nated
Similar to speciation, but cumulatively
greater in intensity; also polyisomerisms, anisomerisms, etc.
Typically large iso-lated units, with speciation pro-
ceeding simultane-ously within units
Bradytelic (slow) and
horotelic (me-dium)
Quantum evolution
May fluctuate greatly; new
variants often rapidly fixed
Pronounced of radi-cal changes in me-
chanical and physio-logical systems
Commonly small wholly isolated
units
Tachytelic (rapid)
However, by the time he had written The Major Features of Evolution (1953), Simpson had changed his view on the nature of quantum evolution and now understood it as “not a different sort of evolution from phyletic evolution, or even a distinctly different element of the total phylogenetic pattern. It is a spe-cial, more or less extreme and limiting case of phyletic evolution.” Gould (1986) argues that this change of heart was brought about by the increasing focus on adaptationism as an evolutionary mechanism at the time. Of course, in the context of the time during which quantum evolution was conceived, the dominant nonadaptive process understood was that of genetic drift, which ar-guably could not bring about the magnitude of the evolutionary patterns that Simpson (1944) described as quantum evolution.
In any case, the function of the nonadaptive nature of quantum evolution at the time still serves as a useful analogue for a discussion on the similarities between his description of quantum evolution and the process of evolution through phenotypic plasticity and consequent genetic assimilation described
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above. It was an attempt to explain how an organism could move from peak to peak in Wright’s (1932) adaptive landscape (Figure 15).
Figure 15. Wright’s (1932) adaptive landscape. The illustration should be read as a topographic map with the geographic coordinates representing various phenotypes and the altitude of the map representing their relative fitness in the environment. To move between two peaks, marked with +, involves crossing valleys of lower fitness and hence poses an evolutionary challenge.
The mechanism through which gradual evolution can occur from one pheno-typic optimum to another remains problematic in evolutionary biology. Simp-son’s (1944) quantum evolution imagined random genetic drift moving the phenotype of an organism sufficiently far away from its adaptive peak that it could survive the shift to another nearby peak. The valley of low fitness be-tween such adaptive peaks is conquered through rapid evolution; according to Simpson (1944) “[quantum evolution] is either completed at a relatively high rate or it is not completed at all, and the population involved simply dies out.” In other words, quantum evolution is the process through which shifts between adaptive zones can occur (Figure 16).
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Figure 16. Quantum evolution from Simpson (1944). The nonadaptive nature of the initial variation generated by quantum evolution facilitates the transition of a lineage from one adaptive zone to an adjacent one, cf. Figure 4.
Evolution via phenotypic plasticity and genetic assimilation has been argued to offer the potential of fulfilling this same function (e.g. Crispo, 2007; Schlichting 2008; Lande, 2009; Schneider & Meyer 2017). Hence this mode of evolution is similar to quantum evolution in both function and characteris-tics (Tables 1 & 2). Also the perceived role of quantum evolution during adap-tive radiations (Figure 17) suggests an affinity of this mode of evolution to the patterns of plasticity and assimilation (Wund et al., 2008; Pfennig et al., 2010; Schneider & Meyer 2017). For this reason I argue that patterns in the fossil record predicted to result from evolution via phenotypic plasticity and genetic assimilation are not only relatively straightforward to identify, but also in fact have a history of analysis in other frameworks and by other names.
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Figure 17. “Explosive” evolution from Simpson (1944). Multiple “quantum steps” resulting in a radiative burst of evolution only to subside and for evolutionary stasis to return in each of the generated lineages.
Summary The conceptualization of the level at which natural selection occurs is more than a simply semantic argument. It draws attention to the complex nature of the relationship between phenotype, genotype and environment (Budd, 2006; Schneider & Meyer, 2017). While the EES has laid the foundation for a theo-retical framework in which to study these complexities (Laland et al., 2015), some of the processes resulting from these interactions, such as phenotypic plasticity and genetic assimilation, have proven challenging to study. While Pigliucci & Murren (2003) caution that “given the hypothesis that [genetic] assimilation can occur within a few generations, it ironically may be too fast for us to catch”, there is in fact a history of the predicted patterns of this mode
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of evolution being analysed albeit in different contexts. The predicted results of evolution via plasticity and assimilation are evolution occurring chiefly in two modes: 1. Stabilizing selection during periods of environmental stability leading to
decreasing phenotypic variation and genetic expression but the accumula-tion of CGV.
2. Episodes of phenotypic plasticity induced by environmental stress facili-tating accelerated adaptive shifts and the generation of phenotypic novelty via the release of CGV.
Naturally, the analysis of such patterns in the fossil record will rely on the morphological comparison of similar assemblages of specimens in order to investigate changes in morphology and morphological variability through time as a reaction to perceived environmental stresses. Analyses of this reso-lution are only capable within a framework that understands organismal vari-ation as continuous and not discrete. The outlook for continuing the analysis of the patterns outlined above, as well as reinterpreting earlier work describing essentially identical patterns, within the theoretical framework of the EES is very promising and should constitute a prioritised area of paleobiological re-search going forwards.
Case study In the next section I discuss my work in Papers I and III, which employ mor-phometric methods, as discussed earlier in this thesis, to investigate the mor-phological variation and variability of Agnostus pisiformis, a trilobite-like ar-thropod from the Upper Cambrian, and its close relatives Homagnostus obesus and Trilobagnostus holmi. I illustrate how a quantitative approach to under-standing variation as continuous permits the analysis of subtle patterns of in-tra- and interspecific morphological variation and how the results of such anal-yses provide support for the hypothesized role of phenotypic plasticity and genetic assimilation in evolution.
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The phenotypic plasticity of Agnostus pisiformis
Agnostus pisiformis The Cambrian Series 3 trilobite-like arthropod Agnostus pisiformis is a well-known and much studied organism. It was described already in the early 18th century by von Bromell (1729) and Linnaeus (1747; 1751) but was not named until 1818 (Wahlenberg, 1818). Despite exceptionally preserved juveniles having been recovered (Müller & Walossek, 1979), their phylogenetic posi-tion remains unclear (see Paper I). It is known from a multitiude of localities throughout Sweden (Ahlberg & Ahlgren, 1996) and neighbouring Norway (Høyberget & Bruton 2008) and Denmark (Poulsen 1923) as well as Great Britain (Rushton 1978) and Canada (Hutchinson 1962). In Scandinavia it is present in the Guzhangian Alum Shales, the depositional environment of which is interpreted as either anoxic to euxinic (Thickpenny, 1987) or dysoxic to anoxic (Schulz, 2015). The biostratigraphy and stratigraphy of the Alum Shales has been mapped in detail (e.g. Westergård, 1922) permitting the iden-tification of coeval assemblages across a broad geographic range. Together with its simple morphology (Figure 18) and tendency to be found in abun-dance in assemblages of dislocated cephala and pygidia, this renders them an ideal organism in which to study patterns of morphological variation.
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Figure 18. Agnostus pisiformis from Paper III. Left: Tergal morphology of A. pisi-formis (specimen PMU31693). Scale bar is 2 mm. Right: Illustration of A. pisiformis adapted from Müller & Walossek (1987). The shaded area is the pygidial field; the feature of the organism in which significant morphological variation is detected and explored in Papers I and III.
Intraspecific variation In Paper I assemblages of A. pisiformis (Figure 19) were collected from three Swedish localities and from two separate stratigraphic positions. Using a mor-phometric technique combining EFA and PCA, specimens from these assem-blages were morphologically quantified and compared in a common mor-phospace. Significant intraspecific variation of pygidial morphology was un-covered between coeval assemblages. Detection of these differences was only possible using methods of analysis describing morphological variation as con-tinuous and not discrete, as discussed earlier.
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Figure 19. Agnostus pisiformis from Paper I (A) Typical assemblage of disarticulated cephala and pygidia (B) Cephalon (C) Pygidium. Scale bars are all 2 mm. Specimen PMU 29988.
This variation was interpreted in terms of the theories of stabilizing selection (Schmalhausen, 1949) and genetic canalization (Waddington, 1942). Because the specimens were deposited during the beginning of the Steptoean Positive Carbon Isotope Excursion (SPICE) and concurrent rapid eustatic deepening (Ahlberg et al. 2009), the morphological variation was hypothesized as repre-senting a plastic phenotypic response to dysoxic environmental stress; a likely scenario considering the association between the pygidium and respiratory functions in A. pisiformis (Müller and Walossek, 1987). This is the explicit hypothesis explored in detail in Paper III.
Patterns of phenotypic plasticity and genetic assimilation Paper III examines the hypothetical stress-induced nature of the discovered morphological variation of A. pisiformis. A further set of six assemblages of A. pisiformis as well as one assemblage each of Homagnostus obsesus and Trilobagnostus holmi were collected (Figure 20). Both H. obesus and T. holmi are considered younger members of the same evolutionary lineage as A. pisi-formis, from the Furongian and Cambrian Stage 10, respectively. Similarly as in Paper I, the morphology of the pygidial field of specimens from each as-semblage was quantified using a morphometric approach combining EFA and
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PCA and plotted in a common morphospace. This revealed patterns of varying morphology as well as morphological variability between the assemblages.
Figure 20. Pygidia of agnostids studied in Paper III (A) Agnostus pisiformis, speci-men PMU31694 (B) Homagnostus obsesus, specimen SGUR11017 (C) Trilobagnos-tus holmi, specimen SGU9843. The scale bar is 2 mm.
In order to investigate whether or not these patterns were correlated with en-vironmental stress, samples of the rocks from the assemblages of A. pisiformis and H. obesus were geochemically analysed and their Mo, U and V contents measured. These heavy metals can be used as proxies for anoxic/euxinic con-ditions of the depositional environment (Emerson & Huestad, 1991; Schovsbo, 2002; Tribovillard et al., 2006). We identified significant correla-tions between both pygidial morphology and pygidial morphological variabil-ity and dysoxic stress (Figure 21A&B). Specifically we found that with in-creasing environmental stress, assemblages exhibited both a morphology in-creasingly similar to that of H. obesus (Figure 20) as well as greater morpho-logical variability. We interpret these results as indicating the presence of environmentally induced phenotypic plasticity in these assemblages.
Furthermore, the morphological variability of T. holmi, the youngest or-ganism of the evolutionary lineage studied, is significantly lower than that of the other assemblages (Figure 21C). This is important because the environ-mental perturbations of the SPICE event had subsided by Cambrian Stage 10, from which this organism is recovered. Consequently, its reduced variability is interpreted as evidence for stabilizing selection occurring and the induced variation becoming genetically assimilated and phenotypically accommo-dated.
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Figure 21. Morphological patterns of assemblages of Agnostus pisiformis, Homag-nostus obesus and Trilobagnostus holmi from Paper III. Numbers adjacent to data points indicate their locality, all assemblages are A. pisiformis unless otherwise stated: (1) Loch Warren (2) Andrarum (3) Jämtland (4) Slemmestad (5) Silverfallet (6) Stånger (7) Risbekken (8) Ringstrand (9) Kakeled (10) H. obesus, Andrarum (11) T. holmi, Andrarum and Hunneberg. See Extended Data Tables 1 & 2 in Paper III for further information on localities and specimens used. Lines represent 95% confidence intervals (A) Relationship between environmental stress and morphology (B) Rela-tionship between environmental stress and morphological variability (C) Relationship between morphology and morphological variability. The blue data point represents T. holmi, interpreted as an organism having undergone stabilizing selection and in which environmentally induced variability has been canalized.
These results provide significant support for the hypothesized process of evo-lution occurring via the induction of phenotypic plasticity followed by genetic assimilation of the uncovered variation discussed earlier. Finally, Paper III concludes with a theoretical model illustrating the manner in which the ob-served patterns are coherent with the predictions of the EES and not the MS (Figure 22).
Figure 22. A population’s response to environmental stress in contrasting theoretical frameworks from Papers III and IV (A) Natural selection causes an adaptive shift of morphology towards a new environmental optimum phenotype according to the Mod-ern Synthesis (B) Phenotypic plasticity induced by environmental stress releases pre-viously cryptic variation and facilitates accelerated adaptive evolution before once again canalizing when reaching a new environmental optimum as per the Extended Evolutionary Synthesis.
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Conclusion
Organismal variation is continuous Although the study of variation occurs today chiefly in discrete terms this is in fact a conceptual bias inherited from the historical development of the field of evolutionary biology and not an empirical reflection of nature. While dis-crete modes of phylogenetic analysis have proved immensely useful in deter-mining the relationship between broad groups of organisms, they struggle to conduct meaningful comparisons of morphologically very similar groups. Adopting a theoretical framework that instead conceptualizes variation as con-tinuous allows for the development of novel modes of analysis making possi-ble the investigation of previously inaccessible patterns of variation. In the field of palaeontology, this is achieved through the use of morphometric meth-ods that permit the analysis of morphological variation in the fossil record at a much higher resolution than before.
In Paper II, such methods are successfully employed to analyse the mor-phological and ontogenetic variation of Mackinnonia. The results of this anal-ysis are used to develop the concept of incipient species, defined as: “popula-tions (or assemblages) of a species that exhibit minor or no morphological differences in terms of characters but significantly different morphology in quantitative terms.” (Paper II).
Papers I and III also use such methods in order to investigate patterns of intra- and interspecific morphological variation in Agnostus pisiformis and its close relatives. These patterns could not have been explored without this the-oretical and methodological approach.
Natural selection acts on the phenotype A framework shift also in terms of the focus of natural selection permits the application of these new methods in exploring novel research questions pre-viously inaccessible within the framework of the MS. While the MS assigns evolutionary primacy to the genotype, the newly emerging EES (Laland et al., 2015) seeks to explore complex relationships between genotype, phenotype and environment. Such relationships are exemplified by the hypothetical oc-
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currence of evolution via phenotypic plasticity and subsequent genetic assim-ilation (Pigliucci et al., 2006). This putative process is explored empirically in Papers I and III and theoretically in Paper IV.
In Paper I, morphometric methods were used to investigate morphological variation in Agnostus pisiformis. Subtle patterns of variation and variability of the pygidium were detected between coeval assemblages in Sweden. These differences were interpreted as potentially the result of environmentally in-duced plasticity as a dysoxic stress response. Paper III explores this hypoth-esis by similarly quantifying morphological variation across coeval assem-blages of A. pisiformis as well as the later organisms of the same lineage Homagnostus obesus and Trilobagnostus holmi. Similar patterns of morpho-logical variation and variability of the pygidium were detected and these pat-terns were found to correlate with geochemical proxies for dysoxic stress. Fur-thermore, the youngest organism of the lineage, T. holmi, was found to exhibit strongly reduced morphological variability, suggesting that it has undergone stabilizing selection.
Consequently, Paper III provides the first empirical support from a spe-cific test in the fossil record for the occurrence of evolution via phenotypic plasticity and genetic assimilation. Furthermore it exposes the notion that mor-phological evolution is either adaptive or ecophenotypic as a false dichotomy; environment and development interact to generate phenotypic variation and evolution.
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Future directions
Morphometrics in the fossil record Combined the two theoretical points made above facilitate the generation of both novel research questions in paleobiology as well as the methodologies necessary to investigate them. The development of morphometric modes of phylogenetic analyses should be a focus of palaeontology in order to fully capture the continuous nature of organismal variation. In Papers I, II and III, I have developed one such method combining EFA and PCA in order to quan-tify morphology, morphological variability and ontogeny through time and space. This method is applicable to a broad range of taxa in the fossil record.
Equally, the formation of clear and testable predictions of novel theoretical frameworks, such as the EES, should be a primary goal of palaeobiology mov-ing forwards. Paper IV is an example of progress towards this goal. It con-textualizes the EES in palaeontology, focusing specifically on the process of evolution through phenotypic plasticity and genetic assimilation, and outlines what are the predictions of such a process in the fossil record and how these ought to be tested.
The fossil record offers enormous potential to provide data informative for novel theoretical notions of evolutionary patterns provided testable predic-tions are drawn up and suitable methodologies developed.
Cambrian explosion The theoretical framework of the EES and its bearing on the relative roles of the genotype, phenotype and environment in evolution have significant impli-cations for the study of the Cambrian explosion and early metazoan history. While the Cambrian explosion is typically considered to represent the sudden emergence of the modern phyla, it is becoming increasingly clear that meta-zoans in fact originated earlier in at least the Late Ediacaran (Valentine et al., 1999; Sperling et al., 2010; Erwin et al., 2011) and that the organisms de-scribed by e.g. Gould (1989) as extinct phyla in fact represent stem-group members of the extant phyla (Budd & Jensen, 2000). Regardless of when pre-cisely the major animal groups appeared, the Cambrian explosion was un-doubtedly a period of high diversification rates, whether uniquely high
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(Bowring et al., 1993) or comparable to later radiative events (Lieberman, 2003).
The likely causes of the Cambrian explosion and the dynamics of the fol-lowing diversification are sources of much speculation. Explanations tend to-wards one of two increasingly intertwined schools of thought; the ecological and developmental, each focused on its own form of evolutionary mechanisms and constraints. Suggested ecological causes range from abiotic factors such as ocean chemistry (Peters & Gaines, 2012) to organismal interaction and competition (Marshall, 2006) to morphological traits (Parker, 2003). What-ever the imagined cause, the idea is that environmental checks ultimately limit the radiation event. Knoll (2003), for example, discusses ecological niche-fill-ing in this context. In the developmental school of thought, organisms are con-sidered more evolvable early in their evolutionary history and become increas-ingly less so as evolution occurs. Davidson & Erwin (2006), for example, highlight the role of the necessary preservation of GRNs underlying body plan development in limiting further phyletic evolution at a scale comparable to that of the Cambrian explosion.
Naturally, all of the factors mentioned above are likely to play their part in structuring the evolutionary patterns of the Cambrian explosion. Yet it is be-coming increasingly clear that the notion of either environmental or develop-mental causes and constraints being responsible for structuring evolution rep-resents a false dichotomy. Progress in our understanding of the Cambrian ex-plosion is likely to occur through research carried out in the theoretical frame-work of the EES, which seeks not to simplify but to clarify and understand the interactions and relative roles of environment and development in evolution.
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Svensk Sammanfattning
Introduktion Den modern evolutionära syntesen (MES), eller nydarwinismen som den också kallas, utgör den nuvarande dominanta teoretiska ramverket inom vilket evolutionsbiologisk forskning sker. MES kännetecknas av den primära rollen som tillskrivs genotypen i evolutionära processer och mönster; i slutänden kan alla evolutionära observationer och tolkningar härledas till förändringar i gen-populationer. Ett alternativt förhållningssätt till evolutionen håller samtidigt på att växa fram: den utökade evolutionära syntesen (UES) betonar istället vikten av komplexa mönster av interaktioner och ömsesidig kausalitet i evo-lutionära processer. Exempelvis förstås miljön utöva inflytande över utveckl-ingsbiologiska processer likväl som genomet.
Bland de mer kontroversiella förutsägelserna som UES framhäver är feno-typisk plasticitet och genetisk assimilation. Fenotypisk plasticitet definieras som förmågan av samma genom att utveckla varierande fenotyp beroende på signaler från omgivningen. Fenotypisk plasticitet i sig är ett någorlunda väl-känt fenomen, men rollen vilken UES tillskriver denna process i evolutionen är det som är kontroversiellt.
Relationen mellan genotyp och fenotyp är det centrala i denna kontrovers; medan MES förstår denna relation som ensidig, dvs. att genotypen kodar för en fenotyp som sedan skapas under utvecklingen, så förespråkar UES en mer flexibel relation. Denna relation har att göra med hur kanaliserad en genotyp är. Under förutsättningarna att en population organismer är välanpassade till sin omgivning så sker selektion för återskapandet av samma fenotyp. Detta gör att de organismer som bäst kan isolera sin genotyp från samtliga potenti-ella störningar, både miljömässiga sådana samt interna genotypiska variat-ioner och förändringar, är de som för sina gener vidare. Detta leder till en population organismer vars utveckling alltid upprepar sig på samma vis; dessa kallas för starkt kanaliserade organismer. Denna kanalisering har dock en si-doeffekt; när genotypen kanaliseras kan den också förstås som skyddad mot förändringar. Organismen utvecklas alltid likadant oberoende av signaler från miljön vilket gör att de slumpmässiga genetiska variationer som uppstår inte selekteras bort. Eftersom utvecklingen är så starkt kontrollerad så får denna variation aldrig visa sig och blir därför aldrig bortselekterat. Detta gör att ka-naliserade organismer samlar på sig kryptisk genetisk variation (KGV). Det är detta KGV som tillskrivs en viktig roll i evolutionens gång inom UES.
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Evolution genom fenotypisk plasticitet och genetisk assimilation Det KGV som samlar på sig i organismer kan förstås som kapacitans. Trots att dessa organismer besitter stor genetisk variation uttrycks den inte, just där-för kallas den kryptisk. Men om organismerna utsätts för starka miljöstress så kan KGV:n utlösas. I sådana situationer uppvisar organismerna en starkt vari-abel fenotyp då många genetiska förändringar kan ha ackumulerats under ti-den de inte uttrycktes. Detta gör att när denna evolutionära kapacitans utlöses så kan både adaptiva och icke-adpativa evolutionära mönster uppenbara sig. Detta gör dessutom att organismer kan förflytta sig snabbt genom adaptiva landskap, dvs. att fenotyper som kan vara fördelaktiga men som inte skulle kunnat evolveras gradvis kan infinna sig i en population. Cykler av samlande av KGV under perioder av lugna miljöförhållande följt av utlösning av denna kapacitans påstås av UES kunna utgöra en primär process genom vilken org-anismer evolveras. I synnerhet betonas vikten av en sådan hypotetisk process vid adaptiva radiationer. Genetisk assimilation är den processen där fenoty-pisk variation som genererats genom fenotypisk plasticitet assimileras in i ge-nomet på organismer. Med andra ord, den processen där miljön gör att organ-ismer uppvisar variation och sedan selekterar bland denna nya variation.
Variation som ett kontinuerligt spektrum Medan forskning pågår på denna process inom biologiska fält så har paleon-tologin ännu inte kunnat bidra. En av anledningarna till att forskning på feno-typisk plasticitet i det fossila registret inte ännu skett är en brist på analytiska metoder som är kapabla till att upptäcka de mönster av morfologisk variation som förutsägs av en sådan process. Eftersom plasticiteten som beskrivs ovan uttrycks inom en art snarare än mellan två eller flera arter innebär det att me-toder för att studera intraspecifik variation måste först utvecklas innan man kan studera denna process.
Sådana metoder utgör en kontrast mot de mest vanligt använda metoderna inom paleontologisk forskning idag. Kladistiska analyser, som utgör merpar-ten av fylogenetiska undersökningarna som sker idag, beskriver morfologisk variation i form av närvaro eller avsaknad av ett antal karaktärer. En matris byggs upp över mönster av närvaron eller avsaknaden av dessa karaktärer inom en mängd olika organismer och denna analyseras sedan på olika vis för att härleda vilka grupper har med störst sannolikhet fylogenetiska band.
Ett alternativ till dessa metoder utgörs av morfometriska metoder såsom landmärkesanalyser och konturanalyser. Dessa beskriver istället morfologisk variation som numeriska värden längs med kvantitativa spektra. De kan med andra ord avläsa betydligt mindre uppenbara morfologiska variationer och är därför väldigt lämpliga för undersökning av fenomen såsom fenotypisk plas-ticitet där morfologiska skillnader mellan olika grupper förväntas vara liten.
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Morfologisk variation hos Mackinnonia I Artikel II utvecklar jag just sådana metoder och tillämpar de för att analy-sera morfologiska variationen hos Mackinnonia, ett släkte kambriska blötdjur. Jag kvantifierar morfologin hos tre grupper av Mackinnonia; två grupper av Mackinnonia rostrata och en grupp Mackinonnia taconica. Genom att jäm-föra formen av individer från dessa tre grupper kan jag konstatera att det finns signifikant intraspecifik variation inom M. rostrata. Därför fortsätter Artikel II med en teoretisk diskussion om samt revision av artbegreppet inom paleon-tologin. Min medförfattare och jag lanserar begreppet begynnandeart för att beskriva två grupper av tillsynes samma art som saknar kvalitativa skillnader i termer av karaktärer eller egenskaper men som ändå uppvisar signifikanta skillnader morfologiskt i kvantitativa termer.
Fenotypisk plasticitet och genetisk assimilation hos Agnostus pisiformis I Artikel I och III undersöker jag den morfologiska variationen hos Agnostus pisiformis, och i Artikel III dessutom även två närbesläktade arter. A. pisifor-mis är ett trilobit-liknande leddjur från kambrium i Sverige. Dessa bevaras i alumskiffern genom stora delar av Sverige såsom Andrarum i Skåne, Kinne-kulle i Västergötland, kring Brunflo nära Pilgrimstad i Jämtland samt även i Norge, Danmark, Wales och Kanada.
Stenarna varifrån A. pisiformis samlas har beskrivits omfattande och det existerar därför stark stratigrafisk kontroll över stenar innehållande A. pisifor-mis från olika lokaliteter inom och utanför Sverige. Detta gör att man kan jäm-föra samlingar av A. pisiformis från olika lokaliteter och vara säker på att man jämför organismer från samma tid. Just detta gjorde jag i Artikel I där jag undersökte samlingar av A. pisiformis från tre lokaliteter i Sverige och upp-täckte spår av intraspecifik variation även hos A. pisiformis. Denna variation i svansen tolkades hypotetiskt vara resultatet av evolutionär stress; somliga lokaliteter må ha haft mindre syre än andra vilket föranledde en stressinduce-rad evolution där svansens yta för respiration maximerades.
För att undersöka denna hypotes samlades stenar in från ännu fler lokali-teter med A. pisiformis och dessutom även en lokalitet vardera med Homagnostus obesus och Trilobagnostus holmi, två närbesläktade arter som finns i stratigrafiskt yngre stenar. Dessa organismer analyserade jag morfo-metriskt i Artikel III. I denna artikel mättes även mängden uran, molybden och vanadium i stenarna varifrån vi fick fossilerna. Mängden uran, molybden och vanadium kan användas som ett mått på den relativa nivån av dysoxisk stress som infann sig då sedimentet formades, dvs., hur pass stressade organ-ismerna var då de levde.
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Dessa mätningar gjorde att vi kunde konstatera att de observerade morfo-logiska skillnaderna mellan A. pisiformis från olika lokaliteter faktiskt sanno-likt orsakades av dysoxisk stress. Dessutom kunde vi visa att den senare org-anismen H. obesus representerar en ännu mer stressad form av A. pisiformis samt att T. holmi representerar en ännu senare form av samma organismer men som inte längre är stressad och därför uppvisar förminskad morfologisk vari-ation.
Vi relaterade dessa slutsatser till konceptet evolution genom fenotypisk plasticitet och genetisk assimilation som nämndes ovan och fann att det var just denna process som med allra största sannolikhet skedde hos A. pisiformis och dess senare former.
Slutsatser och framtidsutsikter I Artikel IV relaterar jag UES specifikt till paleontologi och uttrycker exakt vilka mönster som förutses av processen evolution genom fenotypisk plastici-tet och genetisk variation i det fossila registret. Dessutom belyser jag lämpliga metoder för att undersöka denna process.
Det fossila registret har inte undersökts med noggrannhet i sökandet efter spår av denna process så utsikterna är mycket lovande att med rätt morfomet-riska metoder kunna identifiera flera fall där denna process skett och generera mer empiriskt stöd för UES.
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Acknowledgements
I have had the enormous privilege of conducting my PhD under the supervi-sion of my main supervisor and dear friend Graham Budd, for which I am very grateful. I am thankful for having been afforded the opportunity to pursue ideas and concepts of my own interest and for having received help and guid-ance in developing and structuring these into meaningful and relevant re-search. I am also thankful for the co-supervision of Jorijntje Henderiks and Richard Mann, who have always been available to provide feedback and ad-vice. My work was funded by the Swedish Research Council (VR) grant no. 621-2011-4703 to Graham Budd.
The Palaeobiology Programme at Uppsala University is a friendly and open research environment and I am happy to have always had the opportunity to discuss my work as well as other research with everyone there including John Peel, Lars Holmer, Ralf Janssen, Sebastian Willman, Ben Slater, Åsa Frisk, Magnus Hellqvist and Manuela Bordiga.
I would especially like to thank Malgorzata Moczydlowska-Vidal for her many constructive and critical comments and questions as well as our always thought-provoking theoretical conversations, Nicolàs Campione for his use-ful advice and patient explanations of morphometric methodologies, and Mi-chael Streng for his generous instruction and practical help with specimen preparation, field work, equipment and logistics.
Thanks also to my fellow PhD students Aodhan, Oskar, Heda, Haizhou, Luka, Mattias, Wendy, Lewis, Emma, Xiadong and Zhiliang for their sup-port over the years.
I am especially grateful to Giannis, Tom and Linda for their close friend-ship and our many stimulating and rewarding yet mostly hilarious scientific, methodological, philosophical, historical, political, cultural, musical, literary, cinematic, culinary, (etc.) arguments, agreements, disagreements, debates and laughs.
Thank you to the efficient and communicative administrative staff of the department. In particular, thank you to Ingegerd, Fatima and Siv for their extensive help with various tasks throughout my PhD. Thank you also to my friends Faranak, Kristina, Paula, Negin and Golaleh who have welcomed me with a smile every morning and provided me with the coffee required to complete this thesis.
I am grateful for the many people who have helped provide specimens for my research through field work, examination of museum collections or
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through donations. These include Michael Streng and Mark Wolvers for their help collecting specimens in the field, Jan Ove Ebbestad for his help at the Museum of Evolution of Uppsala University, Linda Wickström at Sveri-ges Geologiska Undersökning, Christian Skovsted at the Swedish Museum of Natural History, Matthew Ridley at the Sedgwick Museum of Earth Sci-ences and Magne Høyberget for his incredibly kind donation of specimens from Norway.
Thank you to my co-authors Tom Claybourn and Madeleine Bohlin with whom it was a pleasure to work and write.
I would like to thank Göran Arnqvist for his help with my project, both through his teaching and for kindly agreeing to act as the opponent for my licentiate thesis. His methodological suggestions and critical comments ben-efited my research enormously. Thank you also to David Gee, who gener-ously shared of his abundant knowledge of the Swedish Alum Shales. I am grateful also for the helpful guidance and friendly comments of Glenn Brock.
During my graduate education at Uppsala University I was fortunate to have been lectured by many extremely helpful and knowledgeable teachers, for which I am very thankful. I would like to thank in particular Mikael Thol-leson and Henning Blom who both greatly helped me structure my under-standing of evolution.
I thank Linda Elvingson for her friendship and her continually skeptical attitude towards this thesis, which has prompted much valuable reflection.
I am lucky to have an enormous and enormously supportive and loving family. To my Mum, Fenella, thank you for unwaveringly and uncondition-ally supporting me – I’m here because of you. Thanks to my Dad, Paul, for always making the time for the patient, educational and stimulating discus-sions that have made me who I am.
Thank you Vic for kindly and gently reminding me to reject all bias and not to discount any hypothesis prematurely.
I appreciate the lovingly feigned interest of my siblings Tom, Sophie, Fred and Björn over the years and for their constant support. Thanks especially to Ryan for his enthusiastic and helpful feedback as I was writing this thesis. Thank you to Kai and Mikki for always being available to help and cheer me along and to Kane for our interdisciplinary discussions. Thanks to fellow Shenton whags Yasmine and Lilly and to my in-laws Rolf, Linda, Ron and Betty.
Lastly, and most of all, thank you Steph; I truly could not have done this without your love and encouragement.
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